Genetic characterization, age and reproductive status of dwarf sperm whales (Kogia sima) stranded along the Italian coastlines


Published: Jul 5, 2024
Keywords:
Cetacea Kogiidae Mediterranean Sea mitochondrial DNA age estimation gonadal histology
NICOLA MAIO
TATIANA FIORAVANTI
LUCREZIA LATINI
AGNESE PETRACCIOLI
MARCELLO MEZZASALMA
GIANNI INSACCO
ANDREA SPLENDIANI
FRANCESCO POLLARO
FABIO MARIA GUARINO
VINCENZO CAPUTO BARUCCHI
Abstract

The knowledge of the life history traits of cetaceans, especially in the case of species that are difficult to observe in the wild, often benefits from the study of stranded individuals. The dwarf sperm whale (Kogia sima) is a vagrant cetacean species in the Mediterranean Sea, which is rarely sighted in water and occasionally is found stranded along the Italian coasts. In this work, we investigated the genetics, age, and reproductive status of three dead individuals (1 male, 1 female, 1 unsexed), stranded in three different sites along Italian coastlines. We used mitochondrial DNA markers for tracing the geographical origin of the animals, tooth sectioning as a proxy for their age estimation and gonadal histology for evaluating their reproductive status. Genetic analyses revealed that the male and the female are K. sima belonging to the Atlantic clade (A clade). The female, with a total body length (TBL) of 1.95 m, had an estimated age of 12 years, and ovaries with one corpus luteum. The male, with a TBL of 2.07 m, had testicles in late spermatogenesis and an estimated age of 22-24 years. From the unsexed individual, which had an estimated age of at least 20 years, no gonadal samples were obtained as it was stranded as a skeleton. Our findings will contribute to increase the knowledge of some unexplored provenance and life-history traits of K. sima visiting the Mediterranean.

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References
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology, 215 (3), 403-410.
Baccetti, N., Cancelli, F., Renieri, T. 1991. First record of Kogia simus (Cetacea, Physeteridae) from the Mediterranean Sea. Mammalia (Paris), 55, 152-154.
Bandelt, H. J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16 (1), 37-48.
Benchoucha, S., Tamsouri, M.N., El Aamri, F. 2018. First stranding record of Kogia sima (Owen, 1866) in Morocco (Strait of Gibraltar). Journal of the Black Sea/Mediterranean Environment, 24 (2), 175-179.
Bortolotto, A., Papini, L., Insacco, G., Gili, C., Tumino, G. et al., 2003. First record of a dwarf sperm whale, Kogia sima (Owen, 1866) stranded alive along the coasts of Italy. p. 1-8. In: 31st Symposium of the European Association for Aquatic Mammals. Tenerife, Spain, 14−17 March 2003. European Association for Aquatic Mammals, Brussels, Belgium.
Chivers, S.J., Leduc, R.G., Robertson, K.M., Barros, N.B., Dizon, A.E., 2005. Genetic variation of Kogia spp. with preliminary evidence for two species of Kogia sima. Marine Mammal Science, 21 (4), 619-634.
Collareta, A., Cigala Fulgosi, F., Bianucci, G., 2019. A new kogiid sperm whale from northern Italy supports psychrospheric conditions in the early Pliocene Mediterranean Sea. Acta Palaeontologica Polonica, 64, 609-626.
Drouot, V., Berube, M., Gannier, A., Goold, J.C., Reid, R.J. et al., 2004. A note on genetic isolation of Mediterranean sperm whales (Physeter macrocephalus) suggested by mitochondrial DNA. The Journal of Cetacean Research and Management, 6 (1), 29-32.
Evans, K., Kemper, C., McKenzie, J., McIntosh, R., 2007. Workshop on age determination of marine mammals using tooth structure. The South Australian Museum Commonwealth Department of the Environment, Water, Heritage and the Arts, Adelaide, South Australia: South Australian Museum, 74pp.
Fioravanti, T., Maio, N., Latini, L., Splendiani, A., Guarino, F.M. et al., 2022. Nothing is as it seems: genetic analyses on stranded fin whales unveil the presence of a fin-blue whale hybrid in the Mediterranean Sea (Balaenopteridae). The European Zoological Journal, 89 (1), 590-600.
Frantzis, A., 2018. A long and deep step in range expansion of an alien marine mammal in the Mediterranean: First record of the Indian Ocean humpback dolphin Sousa plumbea (G. Cuvier, 1829) in the Greek Seas. BioInvasions Records, 7 (1), 83-87.
Guarino, F.M., Di Nocera, F., Pollaro, F., Galiero, G., Iaccarino, D. et al., 2020. Skeletochronology, age at maturity and cause of mortality of loggerhead sea turtles Caretta caretta stranded along the beaches of Campania (south-western Italy, western Mediterranean Sea). Herpetozoa 33, 39-51.
Guarino, F.M., Di Nocera, F., Galiero, G., Iaccarino, D., Giglio, S. et al., 2021. Age estimation and growth of striped dolphins Stenella coeruleoalba stranded along the coasts of south-western Italy. The European Zoological Journal, 88, 417-424.
Hohn, A.A., Fernandez, S., 1999. Biases in dolphin age structure due to age estimation technique. Marine Mammal Science, 15, 1124-1132. Hohn, A.A., Scott, M.D., Wells, R.S., Sweeney J.C., 1989. Growth layers in teeth from known-age, free-ranging bottlenose dolphins. Marine Mammal Science, 5 (4), 315-342.
Kerem, D., Goffman, O., Spanier, E., 2001. Sighting of a Single Humpback Dolphin (Sousa sp.) Along the Mediterranean Coast of Israel. Marine Mammal Science, 17 (1), 170-171.
Kiszka, J., Braulik, G., 2020. Kogia sima. The IUCN Red List of Threatened Species 2020: e.T11048A50359330. https://dx.doi.org/10.2305/IUCN.UK.2020-2.RLTS. T11048A50359330.en (Accessed 16 June 2023).
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A. et al., 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23 (21), 2947-2948.
Loy, A., Aloise, G., Ancillotto, L., Angelici, F.M., Bertolino, S. et al., 2019. Mammals of Italy: an annotated checklist. Hystrix, 30 (2), 87-106.
Luque, P.L., Learmonth, J.A., Santos, M.B., Ieno, E., Pierce, G.J., 2009. Comparison of two histological techniques for age determination in small cetaceans. Marine Mammal Science, 25, 902-919.
Maio, N., Giovannotti, M., Caputo Barucchi, V., Petraccioli, A., Pollaro, F. et al., 2016. Haplotype characterization of a young stranded Common Minke Whale (Balaenoptera acutorostrata Lacépède, 1804): is the Mediterranean Sea a potential calving or nursery ground for the species? Hystrix, the Italian Journal of Mammalogy, 27 (2), 205-208.
Maio, N., Pollaro, F., Gasparro, A., Petraccioli, A., Mezzasalma, M. et al., 2017. New record of Dwarf Sperm Whale Kogia sima (Owen, 1866) from the Mediterranean Sea (Cetacea Kogiidae). Biodiversity Journal, 8 (4), 947-950.
Maio, N., Pollaro, F., Petraccioli, A., Guarino, F.M., 2022 (Eds). Guida naturalistica di campo ai Cetacei delle acque costiere del Parco Nazionale del Cilento, Vallo di Diano e Alburni. Biologia, eco-logia, distribuzione e conservazione. PNCVDA–Quaderni della Biodiversità n. 2022; Volume 5, Tipografia Carucci Caggiano (Salerno), 314 pp + XXVII.
Maio, N., Fioravanti, T., Latini, L., Petraccioli, A., Mezzasalma, M. et al., 2023. Life History Traits of Sperm Whales Physeter macrocephalus Linnaeus, 1758 Stranded along Italian Coasts (Cetartiodactyla: Physeteridae). Animals, 13, 79.
Manfrini, V., Fioravanti, T., Madonna, A., Maio, N., 2023. First sighting of Gray Whale Eschrichtius robustus (Lilljeborg, 1861)(Cetartiodactyla: Eschrichtiidae) in Italian waters and review of Mediterranean Sea records. Hystrix, the Italian Journal of Mammallogy, 34 (2), 148-151.
Mezzasalma, M., Andreone, F., Aprea, G., Glaw, F., Odierna, G. et al., 2017. When can chromosomes drive speciation? The peculiar case of the Malagasy tomato frogs (genus Dyscophus). Zoologischer Anzeiger, 268, 41-46.
Mezzasalma, M., Andreone, F., Glaw, F., Guarino, F.M., Odierna, G. et al., 2019. Changes in heterochromatin content and ancient chromosome fusion in the endemic Malagasy boid snakes Sanzinia and Acrantophis (Squamata: Serpentes). Salamandra, 55, 140-144.
Murphy, S., Perrott, M., McVee, J., Read, F.L., Stockin, K.A., 2014. Deposition of growth layer groups in dentine tissue of captive common dolphins (Delphinus delphis). NAMMCO Scientific Publications, Vol. 10.
Nagorsen, D.W, Stewart, G.E., 1983. A dwarf sperm whale (Kogia simus) from the Pacific coast of Canada. Journal of Mammalogy, 64, 505-506.
Nishida, S., Uchimura, A., Tajima, Y., Yamada, T. K., 2023. Comparative analysis of the genetic structures of Kogia spp. populations in the western North Pacific. Advances in Marine Biology, 96, 25-37.
Notarbartolo di Sciara, G., 2002. Cetacean species occurring in the Mediterranean and Black Seas. In: G. Notarbartolo di Sciara (Ed.), Cetaceans of the Mediterranean and Black Seas: state of knowledge and conservation strategies. Report to the ACCOBAMS Secretariat, Monaco, February 2002. Section 3, 17 pp.
Notarbartolo di Sciara, G., Kerem, D., Smeenk, C., Rudolph, P., Cesario, A. et al., 2017. Cetaceans of the Red Sea. CMS Technical Series, 33, 86 pp.
Ozbilgin, Y.D., Kalecik, E., Gücü, A.C., 2018. First record of humpback dolphins in Mersin Bay, the Eastern Mediterranean, Turkey. Turkish Journal of Fisheries and Aquatic Sciences, 18, 187-190.
Petraccioli, A., Guarino, F.M., Kupriyanova, L., Mezzasalma, M., Odierna, G. et al., 2019. Isolation and Characterization of Interspersed Repeated Sequences in the Common Lizard, Zootoca vivipara, and Their Conservation in Squamata. Cytogenetic and Genome Research, 157, 65-76.
Piboon, P., Kriengsakpichit, N., Poommouang A, Buddhachat, K., Brown, J.L. et al., 2022. Relationship of stranded cetaceans in Thai territorial waters to global populations: Mitochondrial DNA diversity of Cuvier’s beaked whale, Indo Pacific finless porpoise, pygmy sperm whale, and dwarf sperm whale. Science Progress, 105 (2).
Plön, S., 2004. The status and natural history of pygmy (Kogia breviceps) and dwarf (K. sima) sperm whales off southern Africa, Ph.D. thesis. Grahamstown, Rhodes University, 553 pp.
Plön, S., Baird, S.W., 2021. Dwarf Sperm Whale, Kogia sima. pp 1-14. In: Handbook of the Mammals of Europe. K. Hackländer, F. E. Zachos (Eds). Springer Nature Switzerland.
Plön, S., Best, P.B., Duignan, P., Lavery, S.D., Bernard, R.T. et al., 2023. Population structure of pygmy (Kogia breviceps) and dwarf (Kogia sima) sperm whales in the Southern Hemisphere may reflect foraging ecology and dispersal patterns. Advances in Marine Biology, 96, 85-114.
Read, F.L., Hohn, A., Lockyer, C.H., 2018. A review of age estimation methods in marine mammals with special reference to monodontid. NAMMCO Scientific Publications, 10.
Sambrook, J., Fritsch, E.F., Maniatis, T., 1989. Molecular Cloning: A Laboratory Manual (Volume 3). Cold Spring Harbor Laboratory Press, New York, NY, USA.
Santoro, M., Di Nocera, F., Iaccarino, D., Cipriani, P., Guadano Procesi, I. et al., 2018. Helminth parasites of the dwarf sperm whale Kogia sima (Cetacea: Kogiidae) from the Mediterranean Sea, with implications on host ecology. Diseases of Aquatic Organisms, 129 (3), 175-182.
Tamura, K., Stecher, G., Kumar, S., 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38 (7), 3022-3027.
Untergasser, A., Nijveen, H., Rao, X., Bisseling T. et al., 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research, 35 (2), W71-W74.
Viricel, A., 2012. Using genetics to assess population structure in three cetacean species and to investigate the etiology of cardiomyopathy in Kogia breviceps. Ph.D. Thesis. University of Louisiana at Lafayette, USA.
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